The new generation vessel fired 'lethal munitions' in international waters during a Navy exercised dubbed Digital Talon.
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The US Navy has debuted a "next level" unmanned boat during drills in the Middle East, officials have confirmed.
The newMARTAC T38 Devil Ray USV boat tested firing capabilities with "lethal munitions" in an unprecedented exercise as tensions in the region continue to escalate.
The Navy's Task Force 59 carried out the drill, codenamed Digital Talon. The task force specializes in unmanned tech and Artificial Intelligence.
US Naval Forces Central Command said in a statement that Task Force 59 identified and targeted simulated hostile forces through a method known as "manned-unmanned teaming" before launching live munitions from an unmanned boat and hitting a target vessel.
The Command said the system "successfully scored direct hits each time" but confirmed a human operator oversaw operations, which took place in waters around the Arabian Peninsula.
They added that the operator "made the engagement decisions".
Vice Admiral Brad Cooper said: "We are focused on the operational application of new, cutting-edge unmanned systems and Artificial Intelligence technologies.
"During Digital Talon, we took a significant step forward and advanced our capability to the 'next level' beyond just maritime domain awareness, which has been a traditional focus with Task Force 59.
"We have proven these unmanned platforms can enhance fleet lethality. In doing so, we are strengthening regional maritime security and enhancing deterrence against malign activity."
Adm. Cooper noted the Navy had previously tested unmanned aquatic and aerial vehicles to track Iranian Navy and Islamic Revolutionary Guard Corps Navy ships during routine patrols in the Strait of Hormuz.
The US has boosted its presence in the Red Sea and throughout the Middle East since the start of Israel's war on Hamas on October 8, the day after the fundamentalist group launched an incursion which killed 1,400 Israelis.